From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem

Khadempour, Lily; Kyle, Jennifer; Webb‐Robertson, Bobbie‐Jo; Nicora, Carrie; Smith, Francesca B.; Smith, Richard; Lipton, Mary; Currie, Cameron R.; Baker, Erin

doi:10.1128/msystems.01307-20

Cited by 12 publications

(8 citation statements)

References 44 publications

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“…While further study is needed to resolve the feedback mechanisms enabling protein regulation, cultivar‐derived lipids remain promising candidates for fungal–ant communication given that they can vary across foraged plant fragments (Richard et al, 2004) and can be transferred to the ant's cuticle (Richard, Poulsen, Drijfhout, et al, 2007; Richard, Poulsen, Hefetz, et al, 2007). Moreover, gongylidia are known to be enriched with lipids containing linoleic acid that can elicit foraging responses (inspection, carrying) in leafcutter ants (Khadempour et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

“…Based on the FNN results, we selected P:C diets at the 8 g/L P+C dilution using the diet recipe from Crumière et al (2021). This analysis included a test for the presence of linoleic acid (9,12 octadecadienoic acid (Z,Z)‐, methyl ester, Table S4) due to its previous identification as an important fatty acid metabolized by L. gongylophorus and its association with behavioural modification of leafcutter ants (Khadempour et al, 2021). After 42 days of in vitro growth, fungal tissue was collected from the surface of growth media, flash frozen in liquid nitrogen and stored at −80°C for lipid extractions and analysis with gas chromatography–mass spectrometry.…”

Section: Methodsmentioning

confidence: 99%

“…We further tested the hypothesis that the cultivar reinforces optimized nutritional provisioning by signalling its nutritional needs to its ant farmers. Here, we tested two key predictions: (1) the cultivar signals by synthesizing fatty acid compounds with low volatility that provide information at local scales of small garden patches where mulch is deposited (Khadempour et al, 2021;North et al, 1999;Richard et al, 2004;Sousa et al, 2020), and (2) the cultivar concentrates fatty acids in swollen hyphal cells called gongylidia (bundled into staphylae) that are key nutritional rewards consumed by ants (Mueller et al, 2001;Schiøtt & Boomsma, 2021). We then evaluated the fungal cultivar's role in provisioning its ant farmers by tracking the fate of nutrients beyond the initial substrate deposition stage as they travel through leafcutter farming systems.…”

Section: Introductionmentioning

confidence: 99%

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Reciprocal nutritional provisioning between leafcutter ants and their fungal cultivar mediates performance of symbiotic farming systems

Bolander,

Andersen,

Conlon

et al. 2023

Functional Ecology

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Optimized food acquisition is challenging because foraged diet items are chemically complex and often nutritionally imbalanced. These challenges are likely magnified when foraged foods are used to provision others (e.g. offspring, nestmates, symbionts) with different nutritional requirements. We used a theoretical framework of nutritional niches to study these provisioning challenges in leafcutter ants that cultivate a fungal symbiont with nutrients derived from freshly foraged plant fragments. While the leaf‐cutting behaviours of free‐ranging foragers are well studied, little is known about how colonies use these plant fragments to produce their fungal crop within underground nest chambers. For instance, gardener ants are known to convert vegetation into a nutritional mulch that they plant on the fungus garden. However, it remains poorly understood how the ants use this mulch to target the specific nutritional needs of their fungal crop, and whether the cultivar signals if provisioned mulch meets its nutritional needs. Towards answers, we performed three experiments to assess the precision and specificity of nutritional regulation in farming systems of the Panamanian leafcutter ant Acromyrmex echinatior. A laboratory feeding experiment with nutritionally defined diets showed that ant farmers collect a specific intake target for protein and carbohydrates and then linked strict protein regulation by foragers to the cultivar's fundamental niche for protein. An in vitro experiment with the fungal cultivar in isolation did not detect a signal of protein stress that could be used by the ants to regulate their provisioning behaviour, but it did identify an elevated fatty acid that may reinforce optimal nutritional provisioning if detected by gardening ants. A feeding experiment with isotopically labelled diets then revealed nutrient‐specific and caste‐specific allocation timelines, with nitrogen being assimilated into the cultivar's nutritional rewards before being exclusively consumed by developing brood. In turn, these combined results help resolve the integrated behaviours that give rise to resilient leafcutter farming productivity. We further show how nutritional niches can help disentangle reciprocal provisioning dynamics between symbionts as well as the nutritional transactions that more generally mediate symbiotic stability (e.g. sanctioning, screening, policing). Read the free Plain Language Summary for this article on the Journal blog.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Reciprocal nutritional provisioning between leafcutter ants and their fungal cultivar mediates performance of symbiotic farming systems

Bolander,

Andersen,

Conlon

et al. 2023

Functional Ecology

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“…As they produce this nutritional mulch, it is reasonable to predict that gardeners dynamically detect the needs of their fungal mutualist and provision it with a narrowed version of the broad RNNs collected by foragers (Arenas & Roces, 2016 ; Herz et al, 2008 ). The critical regulatory decision points may thus depend on the cues (Green & Kooij, 2018 ; Khadempour et al, 2021 ) that enable ants to detect their cultivar's immediate nutritional needs and then adjust provisioning.…”

Section: Discussionmentioning

confidence: 99%

The multidimensional nutritional niche of fungus‐cultivar provisioning in free‐ranging colonies of a neotropical leafcutter ant

et al. 2021

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Foraging trails of leafcutter colonies are iconic scenes in the Neotropics, with ants collecting freshly cut plant fragments to provision a fungal food crop. We hypothesised that the fungus‐cultivar's requirements for macronutrients and minerals govern the foraging niche breadth of Atta colombica leafcutter ants. Analyses of plant fragments carried by foragers showed how nutrients from fruits, flowers and leaves combine to maximise cultivar performance. While the most commonly foraged leaves delivered excess protein relative to the cultivar's needs, in vitro experiments showed that the minerals P, Al and Fe may expand the leafcutter foraging niche by enhancing the cultivar's tolerance to protein‐biased substrates. A suite of other minerals reduces cultivar performance in ways that may render plant fragments with optimal macronutrient blends unsuitable for provisioning. Our approach highlights how the nutritional challenges of provisioning a mutualist can govern the multidimensional realised niche available to a generalist insect herbivore.

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“…Gongylidia are swollen hyphae containing vacuoles filled with essential aminoacids, lipids, free sugars, polysaccharides, and plant-degrading enzymes ( Quinlan and Cherrett, 1979 ; De Fine Licht et al, 2014 ; Aylward et al, 2015 ). Ants are attracted to the lipids in these specialized structures that compliment adult workers diet and are the sole food source for the ant queen and larvae ( Quinlan and Cherrett, 1979 ; De Fine Licht et al, 2010 , 2014 ; Khadempour et al, 2021 ). Leaf-cutting ants, the most derived higher attines, evolved a sophisticated shift in diet composition and substrate preparation, as they actively cut fresh leaves, flower petals, and fruits to cultivate the fully and highly domesticated Leucoagaricus gongylophorus ( De Fine Licht and Boomsma, 2010 ; De Fine Licht et al, 2010 , 2014 ).…”

Section: Plant-degrading Microbial Communities From Insect Fungiculturementioning

confidence: 99%

Lessons From Insect Fungiculture: From Microbial Ecology to Plastics Degradation

Barcoto

Rodrigues

2022

Front. Microbiol.

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Anthropogenic activities have extensively transformed the biosphere by extracting and disposing of resources, crossing boundaries of planetary threat while causing a global crisis of waste overload. Despite fundamental differences regarding structure and recalcitrance, lignocellulose and plastic polymers share physical-chemical properties to some extent, that include carbon skeletons with similar chemical bonds, hydrophobic properties, amorphous and crystalline regions. Microbial strategies for metabolizing recalcitrant polymers have been selected and optimized through evolution, thus understanding natural processes for lignocellulose modification could aid the challenge of dealing with the recalcitrant human-made polymers spread worldwide. We propose to look for inspiration in the charismatic fungal-growing insects to understand multipartite degradation of plant polymers. Independently evolved in diverse insect lineages, fungiculture embraces passive or active fungal cultivation for food, protection, and structural purposes. We consider there is much to learn from these symbioses, in special from the community-level degradation of recalcitrant biomass and defensive metabolites. Microbial plant-degrading systems at the core of insect fungicultures could be promising candidates for degrading synthetic plastics. Here, we first compare the degradation of lignocellulose and plastic polymers, with emphasis in the overlapping microbial players and enzymatic activities between these processes. Second, we review the literature on diverse insect fungiculture systems, focusing on features that, while supporting insects’ ecology and evolution, could also be applied in biotechnological processes. Third, taking lessons from these microbial communities, we suggest multidisciplinary strategies to identify microbial degraders, degrading enzymes and pathways, as well as microbial interactions and interdependencies. Spanning from multiomics to spectroscopy, microscopy, stable isotopes probing, enrichment microcosmos, and synthetic communities, these strategies would allow for a systemic understanding of the fungiculture ecology, driving to application possibilities. Detailing how the metabolic landscape is entangled to achieve ecological success could inspire sustainable efforts for mitigating the current environmental crisis.

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From Plants to Ants: Fungal Modification of Leaf Lipids for Nutrition and Communication in the Leaf-Cutter Ant Fungal Garden Ecosystem

Cited by 12 publications

References 44 publications

Reciprocal nutritional provisioning between leafcutter ants and their fungal cultivar mediates performance of symbiotic farming systems

Reciprocal nutritional provisioning between leafcutter ants and their fungal cultivar mediates performance of symbiotic farming systems

The multidimensional nutritional niche of fungus‐cultivar provisioning in free‐ranging colonies of a neotropical leafcutter ant

Lessons From Insect Fungiculture: From Microbial Ecology to Plastics Degradation

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